Starch degradation in the bean fruit pericarp is characterized by an increase in maltose metabolism

Abstract The bean fruit pericarp accumulates a significant amount of starch, which starts to be degraded 20 days after anthesis (DAA) when seed growth becomes exponential. This period is also characterized by the progressive senescence of the fruit pericarp. However, the chloroplasts maintained their integrity, indicating that starch degradation is a compartmentalized process. The process coincided with a transient increase in maltose and sucrose levels, suggesting that β‐amylase is responsible for starch degradation. Starch degradation in the bean fruit pericarp is also characterized by a large increase in starch phosphorylation, as well as in the activities of cytosolic disproportionating enzyme 2 (DPE2, EC 2.4.1.25) and glucan phosphorylase (PHO2, EC 2.4.1.1). This suggests that the rate of starch degradation in the bean fruit pericarp 20 DAA is dependent on the transformation of starch to a better substrate for β‐amylase and the increase in the rate of cytosolic metabolism of maltose.

[1]  Jing Wang,et al.  Starch Phosphorylase 2 is essential for cellular carbohydrate partitioning in maize. , 2022, Journal of integrative plant biology.

[2]  Konstantinos D. Tsirigos,et al.  DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks , 2022, bioRxiv.

[3]  P. Coello,et al.  Starch accumulation in bean fruit pericarp is mediated by the differentiation of chloroplasts into amyloplasts. , 2021, Plant science : an international journal of experimental plant biology.

[4]  T. Lawson,et al.  Guard Cell Starch Degradation Yields Glucose for Rapid Stomatal Opening in Arabidopsis[CC-BY] , 2020, Plant Cell.

[5]  J. Ceusters,et al.  Maltose Processing and Not β-Amylase Activity Curtails Hydrolytic Starch Degradation in the CAM Orchid Phalaenopsis , 2019, Front. Plant Sci..

[6]  T. Moritz,et al.  Two-step derivatization for determination of sugar phosphates in plants by combined reversed phase chromatography/tandem mass spectrometry , 2019, Plant Methods.

[7]  B. Zechmann Ultrastructure of plastids serves as reliable abiotic and biotic stress marker , 2019, PloS one.

[8]  Y. Levin,et al.  Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence , 2019, Plant direct.

[9]  N. Kobayashi,et al.  Characterization of high-yielding rice cultivars with different grain-filling properties to clarify limiting factors for improving grain yield , 2018 .

[10]  Jenelle A. Patterson,et al.  Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation. , 2017, Journal of experimental botany.

[11]  M. Stitt,et al.  Leaf Starch Turnover Occurs in Long Days and in Falling Light at the End of the Day1[OPEN] , 2017, Plant Physiology.

[12]  H. Vogler,et al.  Starch Turnover and Metabolism during Flower and Early Embryo Development1[CC-BY] , 2016, Plant Physiology.

[13]  J. Lunn,et al.  A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose1[OPEN] , 2016, Plant Physiology.

[14]  A. Fernie,et al.  Double Knockout Mutants of Arabidopsis Grown under Normal Conditions Reveal that the Plastidial Phosphorylase Isozyme Participates in Transitory Starch Metabolism1[C][W] , 2013, Plant Physiology.

[15]  M. Stitt,et al.  Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate1[W][OPEN] , 2013, Plant Physiology.

[16]  Xuelin Huang,et al.  An improvement of the 2ˆ(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. , 2013, Biostatistics, bioinformatics and biomathematics.

[17]  S. Zeeman,et al.  The Simultaneous Abolition of Three Starch Hydrolases Blocks Transient Starch Breakdown in Arabidopsis* , 2012, The Journal of Biological Chemistry.

[18]  N. Patron,et al.  The Phosphoglucan Phosphatase Like Sex Four2 Dephosphorylates Starch at the C3-Position in Arabidopsis[W][OA] , 2011, Plant Cell.

[19]  J. Roberts,et al.  The role of the pod in seed development: strategies for manipulating yield. , 2011, The New phytologist.

[20]  T. Hahn,et al.  Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana. , 2011, The New phytologist.

[21]  S. Zeeman,et al.  The Laforin-Like Dual-Specificity Phosphatase SEX4 from Arabidopsis Hydrolyzes Both C6- and C3-Phosphate Esters Introduced by Starch-Related Dikinases and Thereby Affects Phase Transition of α-Glucans1[W] , 2009, Plant Physiology.

[22]  M. Steup,et al.  Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. , 2009, Journal of experimental botany.

[23]  Joachim Selbig,et al.  Starch as a major integrator in the regulation of plant growth , 2009, Proceedings of the National Academy of Sciences.

[24]  M. Steup,et al.  The Two Plastidial Starch-Related Dikinases Sequentially Phosphorylate Glucosyl Residues at the Surface of Both the A- and B-Type Allomorphs of Crystallized Maltodextrins But the Mode of Action Differs1 , 2009, Plant Physiology.

[25]  C. Frohberg,et al.  Mass spectrometric quantification of the relative amounts of C6 and C3 position phosphorylated glucosyl residues in starch. , 2008, Analytical biochemistry.

[26]  K. Halliday,et al.  Edinburgh Research Explorer Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts , 2008 .

[27]  Jack A. M. Leunissen,et al.  Turning CFCs into salt. , 1996, Nucleic Acids Res..

[28]  M. Steup,et al.  Phosphorylation of C6‐ and C3‐positions of glucosyl residues in starch is catalysed by distinct dikinases , 2006, FEBS letters.

[29]  Stephen M. Schrader,et al.  Carbon Balance and Circadian Regulation of Hydrolytic and Phosphorolytic Breakdown of Transitory Starch1 , 2006, Plant Physiology.

[30]  T. Sharkey,et al.  Cellular and organ level localization of maltose in maltose-excess Arabidopsis mutants , 2006, Planta.

[31]  P. Geigenberger,et al.  Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under- or overexpress the Pho 2 phosphorylase isozyme. , 2005, Plant & cell physiology.

[32]  P. Coello,et al.  Possible role played by R1 protein in starch accumulation in bean (Phaseolus vulgaris) seedlings under phosphate deficiency. , 2005, Journal of plant physiology.

[33]  D. Thorneycroft,et al.  α-Amylase Is Not Required for Breakdown of Transitory Starch in Arabidopsis Leaves* , 2005, Journal of Biological Chemistry.

[34]  M. Steup,et al.  The glycan substrate of the cytosolic (Pho 2) phosphorylase isozyme from Pisum sativum L.: identification, linkage analysis and subcellular localization. , 2004, The Plant journal : for cell and molecular biology.

[35]  D. Thorneycroft,et al.  A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. , 2004, The Plant journal : for cell and molecular biology.

[36]  Alison M. Smith,et al.  A Previously Unknown Maltose Transporter Essential for Starch Degradation in Leaves , 2004, Science.

[37]  S. Zeeman,et al.  A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. , 1998, The Plant journal : for cell and molecular biology.

[38]  L. Willmitzer,et al.  Antisense inhibition of cytosolic phosphorylase in potato plants (Solanum tuberosum L.) affects tuber sprouting and flower formation with only little impact on carbohydrate metabolism. , 1997, The Plant journal : for cell and molecular biology.

[39]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[40]  M. Stitt,et al.  Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. , 2014, Molecular plant.

[41]  B. Grimm,et al.  Methods for analysis of photosynthetic pigments and steady-state levels of intermediates of tetrapyrrole biosynthesis. , 2011, Methods in molecular biology.